Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication
Abstract Background Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transc...
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doaj-58aca94850bf40708edd64475736db712021-04-18T11:48:25ZengBMCGenome Biology1474-760X2021-04-0122111810.1186/s13059-021-02323-0Comparative regulomics supports pervasive selection on gene dosage following whole genome duplicationGareth B. Gillard0Lars Grønvold1Line L. Røsæg2Matilde Mengkrog Holen3Øystein Monsen4Ben F. Koop5Eric B. Rondeau6Manu Kumar Gundappa7John Mendoza8Daniel J. Macqueen9Rori V. Rohlfs10Simen R. Sandve11Torgeir R. Hvidsten12Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life SciencesCenter for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life SciencesCenter for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life SciencesCenter for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life SciencesCenter for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life SciencesDepartment of Biology, University of VictoriaDepartment of Biology, University of VictoriaThe Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of EdinburghDepartment of Computer Science, San Francisco State UniversityThe Roslin Institute and Royal (Dick) School of Veterinary Studies, The University of EdinburghDepartment of Biology, San Francisco State UniversityCenter for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life SciencesFaculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life SciencesAbstract Background Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80–100 million years ago. Results We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards lower expression and possible pseudogenization. Loss of expression in one ohnolog is significantly associated with transposable element insertions in promoters and likely driven by selection on gene dosage including selection on stoichiometric balance. We also find symmetric expression shifts, and these are associated with genes under strong evolutionary constraints such as ribosome subunit genes. This possibly reflects selection operating to achieve a gene dose reduction while avoiding accumulation of “toxic mutations”. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one likely source of novel binding sites driving tissue-specific gains in expression. Conclusions Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution.https://doi.org/10.1186/s13059-021-02323-0 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Gareth B. Gillard Lars Grønvold Line L. Røsæg Matilde Mengkrog Holen Øystein Monsen Ben F. Koop Eric B. Rondeau Manu Kumar Gundappa John Mendoza Daniel J. Macqueen Rori V. Rohlfs Simen R. Sandve Torgeir R. Hvidsten |
spellingShingle |
Gareth B. Gillard Lars Grønvold Line L. Røsæg Matilde Mengkrog Holen Øystein Monsen Ben F. Koop Eric B. Rondeau Manu Kumar Gundappa John Mendoza Daniel J. Macqueen Rori V. Rohlfs Simen R. Sandve Torgeir R. Hvidsten Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication Genome Biology |
author_facet |
Gareth B. Gillard Lars Grønvold Line L. Røsæg Matilde Mengkrog Holen Øystein Monsen Ben F. Koop Eric B. Rondeau Manu Kumar Gundappa John Mendoza Daniel J. Macqueen Rori V. Rohlfs Simen R. Sandve Torgeir R. Hvidsten |
author_sort |
Gareth B. Gillard |
title |
Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication |
title_short |
Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication |
title_full |
Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication |
title_fullStr |
Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication |
title_full_unstemmed |
Comparative regulomics supports pervasive selection on gene dosage following whole genome duplication |
title_sort |
comparative regulomics supports pervasive selection on gene dosage following whole genome duplication |
publisher |
BMC |
series |
Genome Biology |
issn |
1474-760X |
publishDate |
2021-04-01 |
description |
Abstract Background Whole genome duplication (WGD) events have played a major role in eukaryotic genome evolution, but the consequence of these extreme events in adaptive genome evolution is still not well understood. To address this knowledge gap, we used a comparative phylogenetic model and transcriptomic data from seven species to infer selection on gene expression in duplicated genes (ohnologs) following the salmonid WGD 80–100 million years ago. Results We find rare cases of tissue-specific expression evolution but pervasive expression evolution affecting many tissues, reflecting strong selection on maintenance of genome stability following genome doubling. Ohnolog expression levels have evolved mostly asymmetrically, by diverting one ohnolog copy down a path towards lower expression and possible pseudogenization. Loss of expression in one ohnolog is significantly associated with transposable element insertions in promoters and likely driven by selection on gene dosage including selection on stoichiometric balance. We also find symmetric expression shifts, and these are associated with genes under strong evolutionary constraints such as ribosome subunit genes. This possibly reflects selection operating to achieve a gene dose reduction while avoiding accumulation of “toxic mutations”. Mechanistically, ohnolog regulatory divergence is dictated by the number of bound transcription factors in promoters, with transposable elements being one likely source of novel binding sites driving tissue-specific gains in expression. Conclusions Our results imply pervasive adaptive expression evolution following WGD to overcome the immediate challenges posed by genome doubling and to exploit the long-term genetic opportunities for novel phenotype evolution. |
url |
https://doi.org/10.1186/s13059-021-02323-0 |
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